A socio-ecological framework for examining foodborne parasitic infection risk.

Human liver fluke infection through the consumption of raw freshwater fish is one of the foodborne parasitic infections of global concern. Despite decades of health campaign efforts, high prevalence of infection remains in different areas of the Lower Mekong Basin. This necessitates the consideration of the infection differences between places and the human-environment complexities of disease transmission. This paper used the socio-ecological model as a framework to unraveled the social science dimensions of liver fluke infection. We conducted questionnaire surveys in Northeast Thailand to gather participants' knowledge on liver fluke infection and reasons for raw fish consumption. We synthesized our findings with prior work to identify factors influencing liver fluke infection at four socio-ecological levels. At the individual level, gender and age differences in food consumption habits and personal hygiene of open defection presented the behavioral risks. At the interpersonal level, family tradition and social gathering affected the disease risk. At the community level, physical-social-economic environments of land use and modernization, community health infrastructure and health volunteer support accounted for the varying degree of infection. At the policy level, impacts of regional and national regulations on disease control, health system organization structure, and government development projects were of concerned. The findings provide insights into how infection risks are shaped by people's behavior, social connectedness, interactions with places, and the interplay of these multi-level socio-ecological influences. The framework therefore allows a more comprehensive understanding of liver fluke infection risks to inform a culturally sensitive and sustainable disease control program.

Examining ecosystem (dis-)services on liver fluke infection in rural Northeast Thailand.

BACKGROUND: The direct reliance of humans on and their interactions with freshwater ecosystems in the Lower Mekong Basin have given rise to parasitic infections, which is particularly prevalent in Northeast Thailand where raw fish consumption is practiced. This study examined the interactions between environments, ecosystem (dis-)services, human raw fish consumption habits, and raw fish dish sharing on liver fluke infection risk. METHOD: Water fecal contents and the first intermediate snail host were sampled between June and September of 2019. One hundred twenty questionnaires were surveyed in two villages of different environmental surroundings, one next to a river and the other located inland, in Northeast Thailand. Multivariate regression analyses using linear mixed effect models assessed the influence of social, behavioral and perceptual factors on raw fish consumption frequency, willingness to avoid consumption and liver fluke infection status. Social network analysis compared the degree of raw fish dish sharing between the villages and assessed the probable influence of connections to fish procurement locations and sharing activities on liver fluke infection risk. RESULTS: High abundance of the first intermediate snail host and presence of fecal contamination in water could endanger both villages to ecosystem disservices of parasitic transmission. The river-side village relied more on provisioning ecosystem services than the inland village (29.7% vs. 16.1% of villages) to consume raw fish as their main source of protein. Males in both villages (64.5 and 40.4 days/year for the respective villages) are also likely to consume koi pla and pla som, higher risk fish dishes, more frequently than females (4.1 and 4.3 days/year for the respective villages). The consumption habits of both villages were driven mostly by deriving cultural ecosystem services. Participation in raw fish dish sharing activities significantly reduced the odds of an individual being willing to avoid the consumption (Odds ratio = 0.19). Network analysis suggested that river-side villagers had a more direct raw fish dish sharing interaction and they procured fish from multiple locations; these characteristics might potentially account for more liver fluke infected households in the village. CONCLUSION: Villagers' raw fish consumption is driven by deriving cultural ecosystem services, and the geographic settings of the villages potentially affect villagers' fish procurement locations and infection risk. The findings underscore the linkages between villagers and their surrounding ecosystem environments as pertinent determinants for foodborne parasitic disease risk.

Population dynamics and diversity of trematode infections in Bithynia siamensis goniomphalos in an irrigated area in northeast Thailand.

Several trematodes including Opisthorchis viverrini utilize Bithynia siamensis goniomphalos as a snail intermediate host in their life cycles. In order to capture a comprehensive range of host­parasite interactions and their transmission dynamic patterns, B. s. goniomphalos were sampled monthly over 4 consecutive years in an irrigated paddy-field habitat in northeast Thailand. Using a standard cercarial shedding method, a high diversity of trematodes (17 types) was recovered. Virgulate xiphidiocercariae were the most prevalent (7.84%) followed by O. viverrini (0.71%). In addition to seasonal and environmental factors, the quantity of irrigation water for rice cultivation correlated with transmission dynamics of trematodes in B. s. goniomphalos. The peak prevalence of all trematode infections combined in the snails shifted from the cool-dry season in 2010­2012 to the hot-dry season in 2013 associated with an increasing quantity of water irrigation. A low frequency of mixed trematode infections was found, indicating that the emergence of virgulate cercariae, but not of O. viverrini, was negatively impacted by the presence of other trematodes in the same snail. Taken together, the observed results suggest that interactions between host and parasite, and hence transmission dynamics, depend on specific characteristics of the parasite and environmental factors including irrigated water for rice cultivation.

Effects of Environmental Factors and Infecting Trematodes on the Size and Inorganic Elements of Bithynia siamensis goniomphalos Snails in Northeast Thailand.

Infection with the foodborne trematode, Opisthorchis viverrini, is a major public health issue in southeast Asia. The freshwater snail, Bithynia siamensis goniomphalos, is an intermediate host of O. viverrini and other trematode species. Understanding the effects of environmental conditions and infecting trematodes on B.s. goniomphalos snails is thus crucial for the potential influences on trematode transmission. This study measured environmental variables of water and soil properties, and analyzed B.s. goniomphalos snails for their trematode infection, snail shell length, and inorganic elemental concentration, from 30 localities in northeast Thailand. The results showed that prevalence of trematode infection in B.s. goniomphalos was 3.82%. Nine types of trematode cercariae were identified, with virgulate type 1 as the most common (1.23%). Opisthorchis viverrini-infected snails were mostly found in low-humic gley soils in Sakon Nakhon Province, and were associated with water dissolved oxygen and soil pH. Compared with uninfected snails, larger sizes were observed in virgulate type 1 and pleurolophocerca-infected snails, whereas hypercalcification was noticed in virgulate type 1, virgulate type 3, and pleurolophocerca-infected snails. Infected snails were more sensitive toward environmental conditions, possibly because of the dynamic parasitic processes between trematodes and hosts. Among the environmental factors, soil texture (i.e., sand, silt, and clay compositions) exhibited more significant correlations with B.s. goniomphalos shell characteristics regardless of the trematode infection types. The findings of this study underscore the need to consider the effects of environmental conditions and trematode species-specific pathogenic processes for a more effective and sustainable parasitic control and prevention effort.

Masculinity and misinformation: Social dynamics of liver fluke infection risk in Thailand.

Liver fluke infection through the consumption of raw or undercooked freshwater fish is a major public health problem in the Mekong Region. Despite the extensive efforts of liver fluke health campaigns, Northeast Thailand still reports high human infection prevalence as consumption of raw fish dishes has diminished but not ceased. This study examines the roles of social-cultural factors, particularly the influences of masculinity and misinformation, on liver fluke infection risk. Participant observation, questionnaire surveys and semi-structured interviews were conducted in four villages in Kalasin Province, Thailand, to scrutinize reasons for raw fish consumption, gender differences in raw fish culture, processes of liver fluke information dissemination, and the extent of information mismatch. Our results show that one of the key reasons (76.9%) underlying continued raw fish consumption are deeply embedded cultural practices associated with ways of rural life. About 30% of the participants indicated that they would not avoid eating raw fish, regardless of knowing the health consequences. Gender difference is evident, with 75.6% of males consuming raw fish salad (koi pla), compared to 42.7% of females. Some male participants associate raw meat consumption with virility and strength. Such beliefs underscore the cultural linkage of koi pla consumption with masculinity. Misconceptions of liver fluke life cycle and risk of infection remain, as only 15.3% of the participants correctly selected raw fish as the food source for liver fluke infection while 84.2% misunderstood that other raw foods could lead to infection. The multi-layered and hierarchical structure of public health information dissemination from medical professionals to health officers and village health volunteers to villagers has contributed to information mismatch between different layers. Our study builds on others which call for multi-pronged scientific and social strategies, as well as culturally attuned approaches to public health messaging. The study raises masculinity and misinformation as relevant considerations in disease prevention. Incorporating grounded research and gendered perspectives are part of appreciating the cultural roots of raw fish consumption. Realizing the significant role of village health volunteers in information dissemination and in supplying coherent public health messages is vital for effective health campaigns.

Impact of geography and time on genetic clusters of Opisthorchis viverrini identified by microsatellite and mitochondrial DNA analysis.

Infection by the small liver fluke, Opisthorchis viverrini, causes serious public health problems, including cholangiocarcinoma, in Thailand and southeastern Asian countries. Previous studies have reported that O. viverrini represents a species complex with varying levels of genetic differentiation in Thailand and Lao PDR. In this study, we re-examined population genetic structure and genetic diversity of O. viverrini using extensive samples of the parasite collected over 15 years from 12 geographical localities in Thailand and eight localities in Lao PDR. Parasite life-cycle stages of 721 individuals of O. viverrini (91 cercariae, 230 metacercariae and 400 adult worms) were genotyped using 12 microsatellite loci. Metacercariae exhibited genetic diversity comparable with that of experimentally raised adults: metacercariae can therefore be used to represent O. viverrini populations without the need for laboratory definitive hosts. Data obtained from larval as well as adult worms identified two distinct genetic clusters of O. viverrini. Sequences of a portion of the mitochondrial cox1 gene strongly supported the existence of these two clusters. One, the widespread cluster, was found at all sampled sites. The second cluster occurred only in Phang Khon District, Sakon Nakhon Province (SPk), within the Songkram River wetland in Thailand. A striking feature of our data relates to the temporal dynamics of the SPk cluster, which was largely replaced by representatives of the widespread cluster over time. If the SPk cluster is excluded, no marked genetic differences were seen among O. viverrini populations from Thailand and Lao PDR. The underlying causes of the observed population structure and population dynamics of O. viverrini are not known.

Assessing the role of Filopaludina martensi martensi as a biocontrol agent of Bithynia siamensis goniomphalos, the first intermediate host of Opisthorchis viverrini.

The freshwater snail Bithynia siamensis goniomphalos serves as the first intermediate host of liver fluke Opisthorchis viverrini, a foodborne parasite, of which human infection has persisted in Southeast Asia for decades. The snail Filopaludina martensi martensi has been proposed as a biological control agent against B.s. goniomphalos, but knowledge on the snail ecology and population dynamics between the two species remains rudimentary. This study investigated selected abiotic and biotic factors influencing the distribution and abundance of B.s. goniomphalos and F.m. martensi. Water quality, soils, and snails were collected from 34 localities in Northeast Thailand. Soil properties and snail soft tissue elemental concentrations were analyzed. Experiments were performed to examine interspecific competition. Statistical analysis was conducted to explore the associations between water and soil properties and soft tissue elemental concentrations. The results showed that B.s. goniomphalos had the highest mean dominance in streams and red-yellow podzolic soils, while F.m. martensi snails preferred ponds and latosol soils. Negative correlation in species abundances was found between the two species. Interspecific competition was detected, with B.s. goniomphalos growth rates hampered by the presence of F.m. martensi. Despite the possibility of using F.m. martensi to control B.s. goniomphalos, B.s. goniomphalos exhibited a greater adaptability to different water and soil properties, suggesting that the species could colonize a wide range of environmental conditions. This study provides further insights into the ecology of the two snail species, underscoring the importance of considering abiotic factors when assessing the possible biological control agent to control O. viverrini transmission.

Influence of Water Irrigation Schemes and Seasonality on Transmission Dynamics of Opisthorchis viverrini in the Snail Intermediate Host, Bithynia siamensis goniomphalos in Rice Paddy Fields in Northeast Thailand.

Opisthorchis viverrini is a fish-borne zoonotic trematode that causes significant public health problems in Southeast Asia. Its life cycle requires Bithynia snails as the first intermediate hosts, fish, and human and/or carnivore hosts. This study assessed impacts of land use practice for rice cultivation and seasonality on the transmission dynamics of O. viverrini in Bithynia siamensis goniomphalos in rice paddy field habitats. The transmission of O. viverrini cercariae in B. s. goniomphalos was monitored at monthly intervals over a 4-year period from January 2010 to December 2013. From a total of 59,727 snails examined by standard cercarial shedding, the prevalence of O. viverrini was 0.7% (range, 0.0-4.1%). The prevalence of O. viverrini infection in B. s. goniomphalos varied with the amount of rainfall, with peaks of infection occurring in the cool-dry season, that is, after each rainy season. A shift of peak prevalence from cool-dry to hot-dry season observed in 2013 was associated with the increase in preceding water irrigation to support the production of second annual rice crop. Significant positive correlations were found between the prevalence and intensity of cercarial infection and the size of snails. Our results revealed substantial variation between years so that to have a clear understanding of the population dynamics of this complex system, studies should be conducted over an extended period (> 1 year). Results from this study highlight that water irrigation schemes in rice paddy cultivation and seasonality have a significant effect on the prevalence of O. viverrini in B. s. goniomphalos.

Infection Dynamics of Opisthorchis viverrini Metacercariae in Cyprinid Fishes from Two Endemic Areas in Thailand and Lao PDR.

The infection dynamics of Opisthorchis viverrini metacercariae was analyzed in cyprinid fish from endemic areas in Mukdahan Province, Thailand, and Khammouane Province, Lao PDR. The fish were collected during the cool-dry (November-February), hot-dry (March-May), and rainy (June-October) seasons in 2017. They were examined by the digestion method, and the infection status was statistically analyzed by study area, season, and fish size. The prevalence (no. of fish positive/no. of fish examined × 100) and metacercarial intensities (no. of metacercariae detected/no. of fish positive) of O. viverrini in both study areas depended on season, being high in the cool-dry season and varying in the hot-dry and rainy seasons. In Mukdahan Province, the average prevalence was 18.3% (range 11.0-46.7%, n = 420) and the intensity was 4.07 ± 5.86 cysts/fish (mean ± SD), whereas in Khammouane Province, the prevalence was 51.9% (range 9.1-70.6%, n = 673) and the intensity was 6.67 ± 12.88 cysts/fish. Among the cyprinid fish species examined, the infection was associated with fish body size and predominantly found in Hampala dispar (86.5%), Cyclocheilichthys armatus (73.2%), and Puntius brevis (42.7%). The distribution of O. viverrini metacercariae in fish was skewed, with most of the fish having a low worm burden with an average of four to six cysts/fish. The findings that seasonality, sampling locality, fish size, and species of fish play roles in the risk of O. viverrini infection imply that these host and environmental factors are important for the transmission dynamics and control of O. viverrini.

Culture of fecal indicator bacteria from snail intestinal tubes as a tool for assessing the risk of Opisthorchis viverrini infection in Bithynia snail habitat.

BACKGROUND: Like many trematodes of human health significance, the carcinogenic liver fluke, Opisthorchis viverrini, is spread via fecal contamination of snail habitat. Methods for assessing snail exposure to fecal waste can improve our ability to identify snail infection hotspots and potential sources of snail infections. We evaluated the feasibility of culturing fecal indicator bacteria from Bithynia snail intestinal tubes as a method for assessing snail exposure to fecal waste. Snails and water samples were collected from a site with a historically high prevalence of O. viverrini infected snails ("hotspot" site) and a site with historically no infected snails ("non-hotspot" site) on two sampling days. Snails were tested for O. viverrini and a stratified random sample of snails from each site was selected for intestinal tube removal and culture of gut contents for the fecal indicator bacteria, Escherichia coli. Water samples were tested for E. coli and nearby households were surveyed to assess sources of fecal contamination. RESULTS: At the hotspot site, 26 of 2833 Bithynia siamensis goniomphalos snails were infected with O. viverrini compared to 0 of 1421 snails at the non-hotspot site. A total of 186 snails were dissected and cultured. Escherichia coli were detected in the guts of 20% of uninfected snails, 4% of O. viverrini-positive snails and 8% of snails not examined for cercarial infection at the hotspot site. Only one of 75 snails from the non-hotspot site was positive for E. coli. Accounting for sampling weights, snails at the hotspot site were more likely to have gut E. coli than snails from the non-hotspot site. The concentration of fecal indicator bacteria in surface water was higher at the hotspot vs non-hotspot site on only the first sampling day. CONCLUSIONS: Fecal indicator bacteria can be detected in the intestinal tubes of Bithynia snails. The presence of fecal indicator bacteria in Bithynia snail guts may indicate risk of O. viverrini infection in snail populations. This method has the potential to aid in identifying locations and time windows of peak snail infection risk and may be applicable to other trematodes of human-health significance.

Uncovering the Pathogenic Landscape of Helminth (Opisthorchis viverrini) Infections: A Cross-Sectional Study on Contributions of Physical and Social Environment and Healthcare Interventions.

BACKGROUND: Helminth infections have proven recalcitrant to control by chemotherapy in many parts of Southeast Asia and indeed farther afield. This study isolates and examines the influence of different aspects of the physical and social environment, and uneven intervention effort contributing to the pathogenic landscape of human Opisthorchis viverrini infections. METHODOLOGY: A cross-sectional survey, involving 632 participants, was conducted in four villages in northeast Thailand to examine the impact on prevalence and parasite burden of the reservoir dam environment, socio-economic, demographic, and behavioral factors, and health center intervention efforts. Formalin-ether concentration technique was used for diagnoses, and multivariate models were used for analyses. PRINCIPAL FINDINGS: The importance attributed to O. viverrini infections varied among health centers in the four study villages. Villages where O. viverrini infections were not prioritized by the health centers as the healthcare focus were at a higher risk of infection (prevalence) with odds ratio (risk factor) of 5.73 (3.32-10.27) and p-value < 0.01. Priority of healthcare focus, however, did not appear to influence behavior, as the consumption of raw fish, the main source of O. viverrini infections in the study area, was 11.4% higher in villages that prioritized O. viverrini infections than those that did not (p-value = 0.01). Landscape variation, notably proximity to reservoir, affects vulnerability of local population to infection. Infection intensity was higher in population located closer to the reservoir with risk ratio of 2.09 (1.12-4.02) and p-value < 0.01. Patterns of infection intensities among humans were found to match fish infection intensity, where higher infection intensities were associated with fish obtained from the reservoir waterbody type (p-value = 0.023). CONCLUSIONS/SIGNIFICANCE: This study demonstrated the importance of environmental influence and healthcare focus as risk factors of infections in addition to the socio-economic, demographic, and behavioral factors commonly explored in existing studies. The reservoir was identified as a crucial source to target for opisthorchiasis intervention efforts and the need to consider infection intensity in disease control efforts was highlighted. The holistic approach in this study, which underscores the close relationship between the environment, animals, and humans in development of human infections or diseases, is an important contribution to the framework of One Health approach, where consideration of helminth diseases has largely been overlooked.

Cercarial emergence patterns for Opisthorchis viverrini sensu lato infecting Bithynia siamensis goniomphalos from Sakon Nakhon Province, Thailand.

UNLABELLED: Opisthorchis viverrini sensu lato is a food-borne trematode which is classified as a class 1 carcinogen, with infection potentially leading to cholangiocarcinoma. Snails of the genus Bithynia act as the first intermediate hosts and an amplifying point in the parasite life cycle. In order to investigate seasonal effect on transmission dynamics of O. viverrini in Bithynia siamensis goniomphalos, cercarial emergence and output profiles were monitored at different season. A total of 4533 snails originating from Sakon Nakhon Province, Thailand, collected during the three main seasons, were analyzed for O. viverrini s.l. INFECTION: Emergence of O. viverrini s.l. cercariae from snails was monitored daily from 06:00 to 18:00 h for seven consecutive days. The prevalence of infection in the snails was highest in the hot-dry season and declined in the rainy and cool-dry seasons. Peak cercarial emergence occurred between 08:00 and 10:00 h during the rainy and cool-dry seasons and between 10:00 and 12:00 h during the hot-dry season. The cercarial output was highest in the hot-dry season, similar to a previous study from Lao People's Democratic Republic (PDR). Average cercarial output/snail in Thailand was higher than in Lao PDR. The number of cercariae emerging from the snails was strongly related to snail size, but the relationship between prevalence of infection and snail size differed between seasons. Observed discrepancies in the emergence patterns and per capita cercarial release may reflect differences in environmental, snail, and/or parasite factors particularly biological characteristics between the cryptic species of O. viverrini s.l. and B. s. goniomphalos from Thailand and Lao PDR.

Seasonal transmission of Opisthorchis viverrini sensu lato and a lecithodendriid trematode species in Bithynia siamensis goniomphalos snails in northeast Thailand.

Seasonal changes play roles in the transmission success of fish-borne zoonotic trematodes (FZT). This study examined the seasonal transmission patterns of Opisthorchis viverrini sensu lato (s.l.) and a virgulate cercaria (family Lecithodendriidae) in the snail intermediate host, Bithynia siamensis goniomphalos in northeast Thailand. Snail samples were collected monthly during the rainy, cool, and hot seasons during 2012-2013 to determine the prevalence and intensity of larval trematode infections. The prevalence of O. viverrini s.l. varied significantly with season, being 0.31%, 1.05%, and 0.37% in the rainy, cool, and hot seasons, respectively (P < 0.05). Similarly, the prevalence of virgulate cercariae was 3.11%, 6.80%, and 1.64% in the rainy, cool, and hot seasons, respectively (P < 0.05). The intensity of larval trematode infections also varied between seasons and peaked in the hot season (P < 0.05) in both species. The snails infected with O. viverrini s.l. were significantly smaller (P < 0.05) and those infected with virgulate cercariae were significantly larger (P < 0.05) than uninfected snails. Seasonal variation and the different sizes of B. s. goniomphalos parasitized by O. viverrini s.l. and virgulate trematodes indicate complex host-parasite interactions with important implications for the epidemiology of O. viverrini s.l.

An ecological study of Bithynia snails, the first intermediate host of Opisthorchis viverrini in northeast Thailand.

Infection with the food-borne trematodiasis, liver fluke Opisthorchis viverrini, is a major public health concern in Southeast Asia. While epidemiology and parasitic incidence in humans are well studied, ecological information on the O. viverrini intermediate hosts remains limited. This study aimed to investigate the factors affecting the distribution and abundance of the first intermediate host, Bithynia siamensis goniomphalos snails. Water quality and snails were sampled in 31 sites in Muang District, Khon Kaen Province, Thailand from June 2012 to January 2013 to characterize the B.s. goniomphalos snail habitats. Species relative abundance and Shannon's diversity and evenness indices were employed to describe snail compositions and diversities across different habitat types. Statistical analyses were conducted to examine the extent to which the water quality variables and species interactions account for the relative abundance of B.s. goniomphalos snails. The results showed that the freshwater habitats of ponds, streams and rice paddies possessed significantly different abiotic water qualities, with water temperature and pH showing distinct statistical differences (P<0.05). Different habitats had different snail diversity and species evenness, with high B.s. goniomphalos snail abundance at rice paddy habitats. The differences in snail abundance might be due to the distinct sets of abiotic water qualities associated with each habitat types. The relative abundance of B.s. goniomphalos snails was found to be negatively correlated with that of Filopaludina martensi martensi snails (r=-0.46, P<0.05), underscoring the possible influence of species interaction on B.s. goniomphalos snail population. Field work observations revealed that rice planting seasons and irrigation could regulate snail population dynamics at rice paddy habitats. This study provides new ecological insights into the factors affecting Bithynia snail distribution and abundance. It bridges the knowledge gap in O. viverrini disease ecology and highlights the potential effect of anthropogenic irrigation practices on B.s. goniomphalos snail ecology.